Effects of spatial fragmentation on the elevational distribution of bird diversity in a mountain adjacent to urban areas

Abstract The biodiversity in mountainous ecosystems is high but is threatened by rapid environmental change. Urbanization and other anthropogenic factors in the mountains can affect land use and spatial fragmentation. Moreover, patterns of habitat are closely related to elevation and have a major effect on montane biodiversity. The aim of this study was to analyze the effects of spatial fragmentation on the vertical distribution pattern of bird diversity by characterizing the structure of the bird community, species diversity, and landscape factors at different altitudes. From 2016 to 2019, this study made a four years of continuous monitoring of the breeding birds. The result indicated that Mount Tai harbored a high bird diversity. Bird richness, abundance, and Shannon‐Wiener index decreased with latitude in Mount Tai monotonically. Moreover, the structure of bird communities varied along altitudinal gradients, and some special species were supported in different elevational bands due to the environmental filtering. Road density, number of habitat patches, patch density, and the percentage of forest were significantly related to bird diversity. Sufficient habitat and more patches in the low‐mountain belt supported higher bird diversity. The middle‐mountain belt and high‐mountain belt showed contrasting patterns. Our results highlight the effects of on‐going urbanization and human activities on montane biodiversity and emphasize the need for artificial habitats in the mountains to be managed.

. Over evolutionary time, mountain systems are considered as many of the world's centers and potential refugia of endangered species today, playing a vital role in maintain the high global or regional biodiversity (Antonelli et al., 2018;Hu et al., 2021; Rahbek, Borregaard, Antonelli, et al., 2019a). For example, the European Alps and Qinling Mountains are generally considered to harbor many threatened and endangered animals (Hu et al., 2021;Rahbek, Borregaard, Colwell, et al., 2019b). However, with the rapid development of urbanization and increasing land-use intensity, loss of biodiversity continues at unprecedented rates in human history, especially in tropical mountains (Butchart et al., 2010;Colwell et al., 2004;Peters et al., 2019;Xu et al., 2021). Our understanding of the spatiotemporal maintenance of biodiversity in mountain remains poor, relatively little is known about how land-use change and human activities influence biodiversity along elevational gradients.
Thus, this study was designed to figure out the mechanism that how the habitat fragmentation affect biodiversity along elevational gradients in the context of urbanization. With the decline in terrestrial biodiversity, understanding population structure and spatiotemporal distribution patterns in mountainous ecosystems is important for formulating conservation strategies (Barbier et al., 2018).
There are many valuable studies illustrating the impacts or mechanism of different environmental factors on biodiversity, and the elevational change of biodiversity has always been a research hotspot over recent decades (Colwell et al., 2004;Rahbek, Borregaard, Colwell, et al., 2019b). In mountainous areas, there is a vertical gradient in species composition because of variation in abiotic conditions. Mountain regions with a high level of geological heterogeneity could support higher levels of species spatial turnover and endemic forms, particularly among plants (Rahbek, Borregaard, Antonelli, et al., 2019a). Multiple environmental factors, such as climate, hydrology, slope, habitat type, man-made interference, and landform, affect distribution patterns of biodiversity in mountainous ecosystems (Jetz et al., 2012;Mccain, 2005). The elevational distribution patterns of insects, moss, bats, birds, vascular plants, and other taxa often show unimodal or monotonic change due to environmental factors (Mccain, 2007b;Song et al., 2015;Tabarelli et al., 1999). Mountain ecology has a potential importance on elevational biodiversity. For example, the topography, climate change, and mineralogical composition in mountain affect the survival of many species, plant physiology, and primary productivity (Emel et al., 2021;Steinbauer et al., 2018;Peters et al., 2019;Rahbek, Borregaard, Antonelli, et al., 2019a;Woodbridge et al., 2021).
Nowadays, the high spatial heterogeneity of ecological and environmental variables characteristic of mountains are suffering the inference of human activities and land use change (Pan et al., 2019;Peters et al., 2019). The level of species diversity and distribution pattern is associated with landscape fragmentation and habitat loss (Emel et al., 2021;Woodbridge et al., 2021). The effect on biodiversity has been exacerbated by the intensification of anthrogenic activities such as deforestation and urbanization, and these have led to significant land-cover changes (García-Llamas et al., 2018;Katayama et al., 2014;Pan et al., 2019). Recent studies and syntheses have increasingly implicated that human activities are strongly related to the changes in biodiversity, at both genetic and species levels (Emel et al., 2021;Woodbridge et al., 2021). Previous study in Andean mountain also demonstrated that human disturbance has been much less extreme in the lowlands, and the diversity of lowland habitats is much higher than it is anywhere along adjacent elevational transects (Butchart et al., 2010;Colwell et al., 2004;Terborgh et al., 1990).
Habitat features, especially that resulting from habitat fragmentation and changes in land utilization, playing an important role in population stability and biodiversity (Fahrig, 2017;Fahrig et al., 2019;Fletcher et al., 2018). Natural habitats are continuously being degraded and lost because of anthropogenic activities, and the ecological mechanisms have become a major focus of research (Butchart et al., 2010;Pereira et al., 2010;Pimm et al., 2014). Tourism, plantation, land development, and species invasion all affect natural habitats and lead to variation in food production, intensity of disturbance, vegetation, and landform (Lele et al., 2020;Peh et al., 2005;Xu et al., 2018). For montane birds, habitat fragmentation and heterogeneity can restrict the ranges of activity, affect levels of biodiversity, and make birds more vulnerable to environmental change (Lele et al., 2020). Continuous observations of birds in New Jiangwan Town in Shanghai have revealed that the mean species abundance (MSA) is strongly negatively correlated with the degree of urbanization and loss of natural habitats (Xu et al., 2018). Multiple hypotheses are developed to explain the spatial-temporal pattern of bird diversity in mountain system, such as mid-domain effect hypothesis, climate hypothesis, space hypothesis, species-area relationship hypothesis, and habitat amount hypothesis (Colwell et al., 2004;Mittelbach et al., 2010;Rybicki et al., 2020).
Human disturbance and habitat fragmentation were rarely considered by these hypotheses. There is thus a need to analyze the effects of human activities and urbanization on bird diversity in mountainous ecosystems (Rybicki et al., 2020).
As montane birds are highly sensitive to habitat changes (Soh et al., 2006), many studies have explored the structure of bird communities and the distribution patterns of montane birds under different degrees of disturbance (Fletcher et al., 2018;Harris & Pimm, 2010;Wu et al., 2010). Habitat environment often shows obvious changes over short distances in mountainous ecosystems, and birds have developed specialized adaptations (Quintero & Jetz, 2018). Rapid spatial changes in landform, vegetation, and disturbance could lead to the changes in the structure, richness, and diversity of bird communities in mountainous areas. Land use and altitude can restrict the distribution of biota and hinder bird activity (Harris & Pimm, 2010;Jetz et al., 2007). The environment at different altitudes strongly affects the ecological, evolutionary, physiological, and protective function of biodiversity (Pounds et al., 1999;Pounds et al., 2006).Functionally similar and closely related montane birds are clustered into groups under the constraints of regional habitats and environmental factors (Fahrig, 2003;Gao et al., 2018;Haddad et al., 2015;Pounds et al., 2006). Some birds tend to live in the high elevation, such as White-bellied Redstart (Luscinia phaenicuroides) in the forest in Mount Tai.
Here, the elevational distribution pattern of birds in Mount Tai is analyzed by integrating data on landscape factors with data on montane biodiversity, and we expect to study the joint effects of human disturbance and habitat fragmentation on biological communities and biodiversity patterns. Elevation gradients in mountain regions are invaluable as a natural laboratory for the empirical testing of the hypothesized framework for biodiversity patterns and their links to human disturbance. This study can be divided into three parts: (1) Based on the continuous field survey, bird data were collected to analyze the community structure, diversity, and distribution pattern of birds. Species, individuals, and disturbance are essential to monitor the variation of bird diversity; (2) To ensure the accuracy and reliability of land-use data, supervision classification was utilized to interpret the remote sensing. The acquisition of landscape matrix was also analyzed by software Fragstats V4.3. What is more, environmental factors, including roads and elevation, were obtained to generate multiscale data; (3) Combined the landscape features and bird data, the relationship between them was characterized at different altitudes. It is necessary to figure out the bird diversity patterns along elevational gradients and the influence of environmental variables on bird diversity.

| Study area
Mount Tai is located in the middle of Shandong Province There are obvious distinctions among the different vertical belts with different climate and vegetation. The habitat types from low to high elevation include deciduous forest, broad-leaf coniferous mingled forest, coniferous forest, and high-mountain scrub-grassland (Wang & Li, 2013). Based on altitude and vegetation, Mount Tai can be separated into three vertical belts: the low-mountain belt (altitude lower than 500 m), middle-mountain belt (altitude from 500 to 1200 m), and high-mountain belt (altitude above 1200 m) (Du, 1985).

| Field survey
In May or June from 2016 to 2019, ten line transects were used to monitor the breeding bird population in Mount Tai. Each transect is 1.5 km in length and 100 m in width. In breeding season of each year, this study organized professional investigators skilled in bird identification to conduct twice field surveys. The average speed of movement along the transect was 1-2 km/h, and the bird species, number of individuals, coordinates, distance to birds, habitat type, threat factors, and altitude were recorded. Detailed survey methods were based on "Technical guidelines for biodiversity monitoring - shtml). Ten line transects were designed to cover the majority of habitat types at different altitudes (L1 ~ L10, Figure 1) and detailed information of each line transects was shown in Table S2. L4 and L5 were set at high altitudes and composed mainly of forest. L2 was set at middle altitudes. L1, L3, L6, and L7 were set from low to middle altitudes and surrounded by forest and shrub. L8, L9, and L10 were set at low altitudes and composed mainly of shrub and construction.  (Table S1). If forest area with tree canopy density is equal or greater than 0.2, the land use is designated as Forest. If forest area with shrub coverage is equal or greater than 40%, the land use is designated as Shrubland. The woodland includes open forest land (forest area with tree canopy density ≥0.1 and<0.2), young afforested land, slash, and nursery garden. Continental water areas, ditches, and hydraulic structures were designated as Water. Artificial habitats were divided into three types based on the usages of land, Tourist area, Construction land, and Undeveloped land.

| Interpretation and environmental variables
To quantify the habitat feature and landscape matrices, we

| Vertical distribution index
Different bird species tended to be associated with different altitudes. We designed the Vertical Distribution Index (VDI) to indicate the selection of altitude for different species in Mount Tai. The numbers 1, 2, and 3 were the weights used for the percentage of the population of birds in the low-altitude zone, middle-altitude zone, and high-altitude zone, respectively.
Vertical Distribution Index (VDI): VDI represents the Vertical Distribution Index of a given species; n L is the observed individual number of special birds in the low-altitude zone; n M is the observed individual number of special birds in the What is more, the index would approaches 2 as well if the species is uniformly distributed.

| Phylogenetic diversity and functional diversity
To calculate phylogenetic diversity, we pruned the global phyloge- To calculate functional diversity, we chose 3 kinds of functional traits: morphological characteristics, feeding habits, and foraging strata Wilman et al., 2014). We calculated phylogenetic signals using Blomberg's K for continuous traits (Blomberg et al., 2003) and statistic D for binary traits (Fritz & Purvis, 2010) to test trait conservatism. The R packages "phytools" and "caper" were used to calculate Blomberg's K (Revell, 2012)

| Statistic analysis
We calculated the total abundance, species richness, and Shannon- The two-way cluster analysis and detrended correspondence analysis were conducted to analyze the relationship among different bird species along elevation using the Sorenson method in software PC-ORD 6.0 (Wild Blueberry Media, LLC).

| Changes in land use along the altitudinal gradient
The composition of land use varied with altitude (Table 1) The area of construction land is the highest in the low-mountain belt because of human activities and urbanization.  (Table S3). Species richness and abundance of birds were highest in forest with 72 species and 3117 individuals (Table S4)

| Distribution pattern of bird diversity along an altitudinal gradient
In Mount Tai, the abundance, richness, and Shannon-Wiener index of birds tended to decrease with altitude ( Figure 4). The richness and abundance in low-mountain belt was highest. Similarly, Faith's PD was significantly highest in low-mountain belt (F 2,78 = 7.10, p < .01), and there was significant difference in FD between low-mountain belt and middle-mountain belt (F 2,78 = 4.66, p < .05) (Figure 5a,b). No significant difference was found in Faith's PD and FD between the middle-mountain belt and the high-mountain belt. SES.PD and SES.
FD also showed a trend of increasing and then decreasing along with altitude gradient (Figure 5c).
The relationships among different bird species were analyzed using a two-way cluster analysis and detrended correspondence analysis ( Figure 6). Diverse land use types leaded to divergent selection favoring different characteristics or activities of birds at different altitudes. Waterbirds were common in the low-mountain belt, but raptor and some rare Passerines appeared in the middle or high mountain belt. Moreover, the value of SES.PD and SES.FD was almost smaller than 0, indicating phylogenetic and functional clustering of bird communities in three vertical belts (Figure 5c). SES.
PD was significantly different from 0, and SES.FD was significantly different from 0 in low-mountain belt and high-mountain belt. There was no significant difference between SES.FD and 0 in middlemountain belt. Based on the features of birds at different altitudes, the structure of the bird community shows a fast turnover as bird diversity decreases with altitude. Moreover, it was also obvious that the landscape pattern have a huge change as elevation increases.
In the low-mountain belt, construction land, water, and woodland supported some species from Anseriformes, Columbiformes,

| Effect of landscape factors on the vertical distribution of birds
Number of patches (Spearman rank correlation, r = −0.43, N = 40, p < .05), and patch density (Spearman rank correlation, r = −0.45, N = 40, p < .05) had a significant negative correlation with elevation, and decreased as the altitude increased ( Figure 7). However, the percentage of forest patches (Spearman rank correlation, r = 0.50, N = 40, p < .05) was positively related to elevation, and increased with increased elevation. Thus, the number of patches, patch density, and roads became more numerous at lower altitudes, which is where the degree of spatial fragmentation was higher.
The correlation between four landscape factors and bird diversity was analyzed to characterize the landscape factors affecting the bird community (Figure 8). Bird richness and the diversity index In some previous study mountain, these studies focused on the interaction of mountain substrates, life forms and climate system and described the relationships among diverse montane environments and biodiversity (Butchart et al., 2010;Colwell et al., 2004;Rahbek, Borregaard, Colwell, et al., 2019b). By contrast, fewer studies have examined the vertical distribution pattern of birds in regions near or inside cities (Pan et al., 2019;Ruggiero & Hawkins, 2008). By the field surveys in Gaoligong Mountains, studies indicated the necessity to promote conservation effort at the low elevation where is high richness of birds but intensive human land use (Pan et al., 2019).
Our findings suggest that there are more habitat types supporting higher diversity in the low-mountain belt. Some species associ-  (Jetz & Rahbek, 2002). The analysis of SES.PD also demonstrates that environmental filtering leads to phylogenetic clustering, especially in the high-mountain belt where SES.PD is lowest. It reflects that selection pressure is highest in the high-mountain belt. Generally, functional diversity of bird communities also decreases along with altitude gradient, which means that less niches are occupied by birds at high elevation gradient. Moreover, the highest SES.FD in middle-mountain belt seems that environmental filtering has little effect on functional diversity in middle-mountain belt.
We think that vacated niches and competitive release are common in middle elevation gradient, leading to less stable functional structure.
The elevational pattern of bird diversity could be driven by multiple factors in Mount Tai surroundeded by cities and farms. Different from four possible patterns of variation in biodiversity along altitudinal gradients (decreasing diversity with increasing elevation; high diversity across a plateau of lower elevations, and then decreasing monotonically; a unimodal pattern with maximum diversity at intermediate elevations; increasing monotonically) (Mccain, 2007a;McCain, 2009;Quintero & Jetz, 2018), abiotic and biotic changes occur within short distances on mountainous gradients in Mount Tai.
The elevational distribution pattern of bird diversity in Mount Tai is consistent with the first model (decreasing diversity with increasing elevation). The vertical distribution of bird diversity along altitudinal gradients is related to multiple factors, such as habitat area, temperature, human activities, and landscape (Colwell et al., 2004;Zhang et al., 2020). This finding implied that diversity is constrained in the high-mountain belt and that there are abundant ecological F I G U R E 5 Phylogenetic diversity and functional diversity of bird communities in different vertical belts. (a) Faith's PD of bird communities in three vertical belts, with the same letter meaning no significant difference. (b) FD of bird communities in three vertical belts, with the same letter meaning no significant difference. (c) Standardized effect size (SES) of Faith's PD and FD of bird communities in three vertical belts. "***" means p-value obtained from onesample t test is less than .001, "**" means p-value is less than .01 niches in the middle and low mountain belt. Due to the rich landscape diversity, the patterns of habitat occupancy and distributional patterns contribute to enhancing biodiversity in the low-mountain belt via the aggregation effect (Kattan & Franco, 2004).

| Mechanism underlying the effects of multiple landscape factors
Mount Tai is a typical montane system that reflects the effect of human disturbance or spatial fragmentation on the vertical distribu-  (Pan et al., 2019;Wambulwa et al., 2021).
Many hypotheses have been proposed to explain elevational distribution patterns of biodiversity. However, mountains surrounding cities have generally been neglected, and most studies do not carefully consider the effect of landscape factors (Kattan & Franco, 2004;Wu et al., 2010). Spatial fragmentation caused by fine-scale and diverse habitats play a vital role in biodiversity and ecosystem health (Pimm et al., 2014;Wilson et al., 2016). Though the result of multiple linear regression analysis demonstrates that elevation have a high effect on bird diversity, the landscape factors have a certain weight. Because of human activity and urbanization, the connectivity and quality of habitat have been greatly compromised (Haddad et al., 2015). There is thus a need to identify the effect of spatial fragmentation on the elevational distribution pattern of birds in mountainous ecosystems faced with urbanization. The "species-area relationship" describing the regular pattern between species abundance and habitat area is one of the core hypotheses of montane ecology (Dengler, 2009;Losos & Schluter, 2000). There is a negative correlation between bird diversity and the patch area of forest, indicating that larger areas of natural habitat correspond to lower bird diversity. This relationship is not consistent with the "species-area relationship." Similarly, the analysis of 150 bird datasets of montane systems revealed that the "species-area relationship" might often not be suitable for explaining the vertical distribution pattern of bird diversity simply (McCain, 2009). The number of patches and patch density are important indicators reflecting spatial fragmentation (Haddad et al., 2015). Compared with previous montane studies, this study found that bird diversity was positively correlated with the number of patches and patch density. However, the number of patches and patch density were negatively correlated with altitude. To make sense of the effects of spatial fragmentation on species richness, the "habitat amount hypothesis" was recently proposed, which notes that what is important is the total amount of habitat in an appropriate spatial extent of the local landscape independent of its spatial configuration (Fahrig, 2013;Fahrig et al., 2019;Rybicki et al., 2020). When the area of habitat is larger, habitat fragmentation may increase species diversity. There is more diverse landscape pattern in low-mountain belt, and the total amount of habitat in Mount Tai is sufficient. The spatial fragmentation in the low-belt mountain with sufficient area is higher than the high-belt mountain and the richness and abundance of birds community in the low-belt mountain is relatively higher. Thus, the "habitat amount hypothesis" may provide a better explanation for the elevational distribution pattern in Mount Tai. Fourth, rich natural resources should be sufficiently utilized to raise ecological awareness. Community, universities, institutes, and government should be connected closely. Public events also should be organized regularly to promote the dissemination of scientific ideas.

| CON CLUS ION
The

ACK N OWLED G M ENTS
The authors are grateful to many volunteers in Mount Tai for their help in the field. The authors are grateful to the Editor and two anonymous reviews for invaluable comments and suggestions that improved the earlier version of this manuscript.

CO N FLI C T O F I NTE R E S T
All authors state that there is no conflict of interest.

DATA AVA I L A B I L I T Y S TAT E M E N T
All data have been archived and made available at https://doi. org/10.5061/dryad.866t1 g1q2.